Glycosylphosphatidylinositol-anchored proteins as chaperones and co-receptors for FERONIA receptor kinase signaling in Arabidopsis

Abstract

The Arabidopsis receptor kinase FERONIA (FER) is a multifunctional regulator for plant growth and reproduction. Here we report that the female gametophyte-expressed glycosylphosphatidylinositol-anchored protein (GPI-AP) LORELEI and the seedling-expressed LRE-like GPI-AP1 (LLG1) bind to the extracellular juxtamembrane region of FER and show that this interaction is pivotal for FER function. LLG1 interacts with FER in the endoplasmic reticulum and on the cell surface, and loss of LLG1 function induces cytoplasmic retention of FER, consistent with transport of FER from the endoplasmic reticulum to the plasma membrane in a complex with LLG1. We further demonstrate that LLG1 is a component of the FER-regulated RHO GTPase signaling complex and that fer and llg1 mutants display indistinguishable growth, developmental and signaling phenotypes, analogous to how lre and fer share similar reproductive defects. Together our results support LLG1/LRE acting as a chaperone and co-receptor for FER and elucidate a mechanism by which GPI-APs enable the signaling capacity of a cell surface receptor.

DOI: http://dx.doi.org/10.7554/eLife.06587.001

eLife digest

Plants respond to changes in their environment by altering how they grow and when they reproduce. A protein called FERONIA is found in most types of cells and regulates many of the processes that drive these responses, such as cell growth and communication between male and female cells. FERONIA sits in the membrane that surrounds the cell, where it can detect molecules in the cell wall and from outside the cell, and send signals to locations within the cell. However, it is not clear how FERONIA is able to specifically regulate different processes to produce the right response in a particular cell at a particular time.

A family of proteins called glycosylphosphatidylinositol-anchored proteins (GPI-APs for short) play important roles in plants, animals, and other eukaryotic organisms. Li et al. studied FERONIA and two closely related GPI-APs called LLG1—which is produced in seedlings, and LORELEI, which is only found in female sex cells . The experiments show that plants missing either LLG1 or FERONIA had similar defects in growth and in how they respond to plant hormones. Plants missing LORELEI had similar defects in their ability to reproduce as the plants missing FERONIA. This suggests that FERONIA works with either LLG1 or LORELEI to regulate similar processes in different situations.

Li et al. found that FERONIA binds to LLG1 in a compartment within the cell called the endoplasmic reticulum—where proteins are assembled—before both proteins are moved together to the cell membrane. In the absence of LLG1, FERONIA fails to reach the cell membrane, and a large amount of FERONIA remains trapped in the endoplasmic reticulum. Therefore, LLG1 acts as a ‘chaperone’ that delivers FERONIA to the membrane where it is required to regulate plant growth. Li et al. found that LORELEI also interacts with FERONIA. Both LLG1 and LORELEI bind to the same region of FERONIA, which is on the outer surface of the cell membrane.

These findings show that FERONIA is able to perform different roles in cells by teaming up with different members of the GPI-AP family of proteins. The next challenges will be to find out if, and how, LLG1 and LORELEI affect the ability of FERONIA to respond to signals from the cell wall and outside the cell.

DOI: http://dx.doi.org/10.7554/eLife.06587.002